Long-term adaptive plasticity regulates the vestibulo-ocular reflex (VOR). Normally, the VOR evokes smooth eye motion that is opposite in direction and equal in amplitude to head motion. However, the system normally operates without feedback and depends on an adaptive mechanism to maintain its excellent performance. In the laboratory, plasticity is achieved by using optics to disrupt the normal relationship between head motion and eye motion. Spectacles that magnify or miniaturize the visual scene cause gradual, semi-permanent increases or decreases in the amplitude of the VOR for a given stimulus. In real life, long-term adaptation of the VOR is critical for maintaining proper motor and perceptual orientation in space, as well as to ensure proper visual acuity during head turns. In addition, an understanding of the neural basis for plasticity of the VOR will provide a model for understanding motor learning and adaptations that are necessary in all motor systems for recovery of function following brain damage and for the maintenance of normal posture and sensory-motor function. The flocculus and ventral paraflocculus of the vestibulo-cerebellum play a critical role for adaptive changes in the VOR. However, the exact function of these structures remains unclear. The research in this proposal will record the electrical activity from single brain cells in the flocculus and ventral paraflocculus of awake rhesus monkeys to resolve important issues concerned the function of the cerebellum in vestibulo-ocular adaptation. First, a concerted effort to sample from previously undersampled regions of the structure will identify groups of Purkinje cells that have not been investigated and reveal the role played by those cells in motor adaptation. Second, electrical stimulation of the vestibular apparatus will identify vestibular pathways to the flocculus and ventral paraflocculus from both labyrinths. Third, comparison of the responses of Purkinje cells to the same electrical stimulus before and after adaptation of the VOR will test directly for an effect of adaptation of the strength and time course of synaptic transmission through specific vestibular pathways to the vestibulo-cerebellum. Finally, recordings from Purkinje cells under conditions that cause adaptive changes in the VOR win reveal whether conditions under which the climbing fiber inputs or simple spike outputs of Purkinje cells are appropriate as teaching signals to guide adaptive changes in the VOR.